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The Effect of Noise Exposure in the Presence of Canal Fenestration on the Amplitude of Short-Latency Vestibular Evoked Potentials
Adi Biron, MD;
Sharon Freeman, PhD;
Jean-Yves Sichel, MD;
Haim Sohmer, PhD
Arch Otolaryngol Head Neck Surg. 2002;128:544-548.
ABSTRACT
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Background Exposure to high-intensity noise causes little, if any, reduction in
vestibular function in normal animals as shown by short-latency vestibular
evoked potentials (VsEPs).
Objective To investigate the effect of noise exposure on VsEPs following fenestration
of the horizontal semicircular canal.
Design and Methods Psammomys obesus (fat sand rat) underwent labyrinthectomy
in 1 ear, while the lateral semicircular canal in the other ear was fenestrated.
Control VsEPs to linear acceleration (approximately 3g;
rise time, approximately 1-2 milliseconds) were recorded immediately after
the operation. The experimental group animals were then subjected to loud
white noise (113-dB sound pressure level) for 1 hour. Immediately after the
noise exposure in the experimental group animals, VsEPs were once more recorded.
Results The VsEPs in the experimental group animals were significantly reduced
immediately following the noise exposure, while there was no change in the
recordings from the control group animals (fenestrated but not noise exposed;
noise exposed but not fenestrated), even though the noise exposure induced
a mean 47-dB threshold elevation of the auditory brainstem response.
Conclusions The presence of the fenestration caused the vestibular end organs to
become vulnerable to noise exposure. The fenestration may create a pathway
enabling pressure release through the vestibular end organs during noise exposure,
thus increasing the possibility of damage to the vestibular end organs. This
did not occur in the intact, nonfenestrated animals.
INTRODUCTION
THE MAMMALIAN inner ear contains an auditory end organ sensitive to
sound and several vestibular end organs that are sensitive to angular and
linear acceleration. Outer perilymph channels and inner endolymph channels
interconnect all end organs. Changes in perilymphatic pressure in response
to a sound stimulus are transmitted throughout these channels to all parts
of the inner ear. The basic sensory unit is identical in all parts of the
inner ear: stereocilia-bearing hair cell, a primary sensory neuron, and the
synapse between them. The transduction mechanism is also identical in all
parts of the inner ear: mechanical changes in the fluids cause bending of
the stereocilia. Bending in one direction causes depolarization of the hair
cell and excitation of the relevant neural pathway, whereas bending in the
opposite direction causes hyperpolarization and inhibition. This structural
and functional similarity between the vestibular and auditory end organs has
led to studies designed to test the possibility that sound stimuli can effect
the vestibular end organs, as originally reported by Tullio1
(known as the Tullio phenomenon). For example, intense sound stimuli (130-172–dB
sound pressure level [SPL]) have been shown to induce reflex eye movements
in guinea pigs and monkeys.2-3
In humans, 125-dB SPL sounds have caused visual field shifts.3
Histological changes in the saccule and additional vestibular end organs following
intense sounds (136-163–dB SPL) have also been reported.4
Also, primary vestibular neurons in cats have been shown to respond to sound
stimuli of intensities 80- to 90-dB SPL.5-6
Clinical studies on healthy humans who had been exposed to noise and humans
during noise exposure reported only subclinical vestibular findings.7-8 However, 17 patients in whom intense
sounds induced vertigo and eye movements have recently been described; in
each of these patients there was an absence of bone (dehiscence) over a portion
of the superior semicircular canal (SCC).9
Over the past few years, a new objective technique for assessing the
vestibular system has been developed: short-latency vestibular evoked potentials
(VsEP), which is a noninvasive method for measuring potentials in response
to acceleration impulses, similar to the technique used to record the auditory
nerve brainstem response (ABR). These potentials were measured first in animals
in response to impulses of angular10 and linear
acceleration11 and later in humans in response
to angular acceleration.12 The first wave (WI)
of the ABR and VsEP represents the compound action potential of those auditory
and vestibular nerve fibers synchronously activated by the respective stimuli
and hence reflects end organ and primary auditory and vestibular nerve function.
These VsEPs have been used in our laboratory to objectively study the
effect of noise on vestibular function in several controlled experimental
paradigms in laboratory animals.13 The animals
were exposed to noise intensities of 113-dB SPL for periods ranging from seconds
to 3 weeks. There was either no effect of these exposures on the VsEPs or
small effects of short duration with recovery.13
Thus, in response to several intensities and durations of noise, little if
any vestibular changes were seen.
It has been suggested that this absence of an effect of high-intensity
noise on vestibular function in normal ears could be because the round window,
which is located in the cochlea, serves as a pressure release in the perilymphatic
channel. Therefore, the sound pressures induced in the cochlear perilymph
by stapes footplate vibration are preferentially transmitted to the perilymphatic
channels of the cochlea and not to the vestibular channels. Hence, most of
the damage is seen in the cochlea. Accordingly, induction of a fenestration
(fistula) in one of the vestibular channels may enable the perilymphatic pressure
wave to be transmitted through this alternative pathway to the vestibular
end organs and make the vestibular end organs also noise sensitive. In fact,
it has been shown in pigeons that fenestration of a semicircular canal makes
vestibular neurons more sensitive to sound.14
In addition, single vestibular neurons of deaf mice began to respond to sound
after fenestration.15
The present study was designed to clarify the mechanism that protects
the vestibular organs from damage caused by exposure to noise. For that purpose,
short-latency VsEPs to linear acceleration were recorded before and after
exposure to high-intensity noise in animals with and without a fenestration
in a semicircular canal.
MATERIALS AND METHODS
ANIMALS
The present study was performed on fat sand rats (Psammomys obesus). Using the sand rat has a major advantage in such
an experiment owing to its unique middle and inner ear anatomy.16
The temporal bone of the sand rat contains an unusually large bulla. Most
parts of the inner ear bulge into the bulla cavity and are easily accessible
for delicate surgical procedures, including fenestration of one of the semicircular
canals. The experiments were conducted in accordance with the guidelines published
by the Hebrew University–Hadassah Medical School Animal Care and Use
Committee.
All of the sand rats were anesthetized by an intraperitoneal injection
of 35 mg/kg of pentobarbital sodium (Nembutal; Abbott Laboratories, Abbott
Park, Ill) solution. Additional anesthesia was administered as required. A
labyrinthectomy was performed on the nontested ear. This was done so that
the recordings would originate from the tested ear only to facilitate interpretation
of the results. Labyrinthectomy also saves the need for masking the other
ear during ABR testing. The VsEP and ABR were recorded at several stages of
the experiments.
VsEP RECORDING
Details of the stimulus and recording techniques have been previously
reported.11 The stimulator comprised a solenoid
coupled to a sliding device to which the animal's head, placed in a head holder
(held between its nasal bone and hard palate), was attached. The device pulled
the head linearly forward (utricle stimulus) with a linear acceleration of
3g and a rise time of 1 to 2 milliseconds (ms). Each
stimulus caused a 50-µm movement of the head and was presented at a
rate of 2 per second. After each stimulus, the head was returned to its original
position at a lower acceleration by springs. The electrical activity was recorded
with subcutaneous E2 platinum needle electrodes (Grass Instrument
Division, Astro-Med Inc, West Warwick, RI) at the vertex referred to the left
ear, with the ground electrode in the right ear. Conventional evoked potential
equipment (Microshev 4000 evoked response system; Microshev Ltd, Efrath, Israel)
was used. The recorded electrical activity in a 12.7-ms poststimulus window
was amplified, filtered (150-3000 Hz), and the responses to the 128 stimulus
repetitions were averaged. The VsEP responses were displayed such that a positive
potential recorded by the vertex electrode appeared as an upward deflected
wave. Throughout all VsEP (and ABR) recordings, body temperature was measured
and maintained at 37°C to 38°C.
ABR RECORDING
An earphone was placed 1 cm from the tested ear, through which a 120-dB
peak equivalent (pe) SPL click was presented at a rate of 20.6 stimuli per
second. Alternating polarity was used to cancel electrical artifacts. The
intensity level was lowered in 5-dB steps until a threshold was reached (ie,
the minimal stimulus intensity at which ABR waves could be identified). At
least 2 readings were taken at every intensity level. Recordings were made
with the same electrodes, sites, filter, average settings, and equipment used
for the VsEP recording.
PARAMETERS
The following response parameters were evaluated: (1) peak-to-peak amplitude
and peak latency of WI of the VsEP to 3g stimulation,
(2) peak-to-peak amplitude and peak latency of WI of the ABR to 120-dB pe
SPL, and (3) ABR threshold. An intensity of 120-dB pe SPL was used to assess
ABR WI because after exposure to the noise, ABR often could not be recorded
in response to lower-intensity stimuli.
NOISE
A Grason-Stadler 455C noise generator (Grason-Stadler Inc, Milford,
NH) connected to an auditory amplifier and a speaker were used to generate
broadband noise. Spectral measurements were made using a precision integrating
sound level meter type 2218 and third octave filter type 1625 (Bruel &
Kjær, Copenhagen, Denmark). The level of noise intensity used was 113-dB
SPL, with a peak at 2 kHz and 14 dB lower in intensity at 250 Hz and 26 dB
lower at 125 Hz.
EXPERIMENTAL PROCEDURE
Following left labyrinthectomy, the lateral SCC of the right ear was
exposed in all animals. The 26 animals studied were divided into the following
4 groups (Table 1):
- Group A (7 animals): the effects of noise exposure
on the VsEPs in the fenestrated ear were examined
- Group B (5 animals): the ear not exposed to noise
was fenestrated to assess possible effects of the fenestration itself on vestibular
function
- Group C (5 animals): the effects of noise exposure
on the VsEPs in the intact (nonfenestrated) ear were examined
- Group D (9 animals): the noise-exposed ear in which
ABR was recorded was fenestrated to evaluate the effects of the noise exposure
on the ABR of the fenestrated ear.
In groups A, B, and D, the bony SCC was fenestrated (size, 2 mm) with
a small drill, taking care not to cause endolymphatic leakage; the SCC was
not fenestrated in group C. The ABR was then recorded in the fenestrated groups
B and D before the noise exposure, and the VsEP was recorded in groups A,
B, and C before exposure. The animals in groups A, C, and D were then exposed
to the 113-dB SPL noise for 1 hour (group B was not exposed to the noise).
Immediately after the cessation of the noise exposure, recordings were again
made of the VsEP in groups A, B, and C and ABR in groups B and D. In the groups
in which both VsEP and ABR were recorded, ABR was recorded first. The VsEP
and ABR were also recorded in the nonexposed group B 1 hour after the first
recording. The VsEP recordings in the fenestrated group A were repeated every
1.25 minutes (approximately) for 30 minutes and again 1 hour after the end
of the noise exposure. The VsEPs in the nonfenestrated group C were recorded
every 1.25 minutes for 10 minutes. The sand rats were then given an intraperitoneal
injection of a lethal dose of pentobarbital. Postmortem recordings were carried
out to prove that the measurements were of a biological source and to rule
out possible electromagnetic or electromechanical artifacts. The animals were
under anesthesia during the entire experiment, from the time of the unilateral
labyrinthectomy until after the postexposure recordings had been made, after
which they were given the lethal dose. The maximal duration of anesthesia
was approximately 2.75 hours. Thus, there was no need to remove the animal
from the head holder and stimulating system between recordings, making the
entire procedure well controlled.
STATISTICS
We used 1-way analysis of variance (ANOVA) to compare amplitude and
latency of VsEP recordings as a function of time in groups A and C. When a
significant (defined as P<.05) correlation was
found, post hoc t tests were used to compare the
2 specific points in time. The nonparametric paired Wilcoxon signed rank test
was used to compare changes in groups B and D.
RESULTS
The ABR response parameters before and after noise exposure were compared
to confirm that the level of noise exposure used (intensity and duration)
was capable of causing auditory (ABR) threshold shifts. The ABR threshold
and the amplitude and latency of ABR WI were compared before and after noise
exposure (1 hour between). The ABR threshold was significantly elevated in
group D after exposure to noise by 47 ± 17 dB (P = .01). The actual average threshold change was higher than this due
to the inability to measure thresholds when they were greater than 120-dB
pe SPL. At 120-dB pe SPL, the latency of ABR WI was significantly prolonged
(P = .02) after noise exposure and amplitude was
reduced, although nonsignificantly. No change was found in the ABR threshold,
WI amplitude, or latency (120-dB pe SPL) in group B, recorded 1 hour apart.
Thus, the noise exposure used in this study induces a clear and significant
threshold elevation of ABR, and the presence of a fenestration for 1 hour
does not affect cochlear (ABR) function.
This same noise exposure in the absence of a fenestration, but following
exposure of the SCC (sham operation, group C), did not have any effect on
the VsEP (WI before, 1.63 ± 0.38 µV; WI after, 1.74 ±
0.70 µV; 1-way ANOVA, F9,30 = 0.35; P
= .95). In addition, the presence of a fenestration, but without noise exposure
(group B), did not effect the VsEP (P = .1), confirming
that the fenestration itself did not have a deleterious effect on vestibular
function.
The most interesting result of this study is shown in Figure 1, in which the amplitude of WI of the VsEP can be seen to
be reduced following noise exposure in the presence of a fenestration. The
mean ± SD peak-to-peak WI amplitude reduction in group A immediately
following the noise exposure was 60% ± 17.32% (P<.001) compared with the preexposure amplitude in each animal. This
reduction was still present 1 hour later (1-way ANOVA, F22,130
= 1.966; P = .01; Figure 2), with a tendency toward partial, though nonsignificant,
recovery. Latency did not change (1-way ANOVA, F22,130 = 0.555; P = .95).
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Figure 1. Vestibular evoked potential (VsEP)
before and after noise exposure. Short-latency linear VsEP recordings before
(3 repetitions above) and immediately after (4 repetitions below) exposure
to 113-dB sound pressure level broadband noise for 1 hour. The intensity of
the linear acceleration stimulus was 3g. Note the
reduction in the amplitude of the first wave.
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Figure 2. Percentage of change in wave I
amplitude. Mean ± SD percent change in peak-to-peak amplitude of wave
I of the vestibular evoked potential as a function of time before (0) and
at several time intervals after the cessation of the noise. Also shown is
the mean percentage of amplitude change of wave I of the major control group
C (noise exposed but nonfenestrated).
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Furthermore, 1 animal showed no change in VsEP recordings after its
SCC was supposedly fenestrated and exposed to noise. In this animal, a postmortem
examination revealed that the fenestration had not been properly carried out
(the bony SCC was not successfully fenestrated). This animal was therefore
excluded from the study.
COMMENT
It is generally accepted that the vestibular end organs are less vulnerable
to high-intensity noise exposure than the cochlea in the intact animal. Several
explanations have been suggested for these findings. First, high-intensity
noise has been shown to cause lower blood flow in the stria vascularis17 and to lower the amplitude of the endocochlear potential.18-19 It is likely that this decreased
strial blood flow is responsible for the lower endocochlear potential. This
would depress cochlear transduction. However, because the endolymphatic spaces
in the vestibular end organs do not have such a positive potential,20 transduction in the vestibular end organs is not
dependent on such a large potential difference across the hair cell. This
would render the vestibular end organs less sensitive to noise.
Second, it has been thought that the vestibular end organs are sensitive
mainly to low frequencies and would not be affected by noise that does not
contain much energy at lower frequencies. However, the noise exposure used
in the present study was broadband, including low frequencies (eg, at 250
Hz, only 14 dB lower from the peak at 2 kHz). In addition, it has been shown
that the vestibular organs can be excited by higher frequency stimulation
because the vestibular stimuli used to elicit the short-latency VsEPs have
high rise times (1-2 ms), ie, comprising high-frequency components (up to
about 250 Hz).
And third, as explained above, the anatomical structure of the inner
ear preferentially directs acoustic energy entering through the oval window
to the cochlea due to the presence of the round window. Hence, most of the
damage would be seen in the cochlea.
The present study was designed to test this last hypothesis, and the
results have clearly shown that SCC fenestration followed by noise exposure
caused a significant reduction in VsEP WI amplitude. Thus, it seems that the
absence of a vestibular "round window" serves to limit stimulation of the
vestibular end organs by acoustic stimuli. Vestibular end organ depression
by the levels of noise used in this study (113-dB SPL for 1 hour) became apparent
only in the presence of a fenestration and were not noted following exposure
to the same noise without fenestrating the SCC. There was a slight nonsignificant
tendency toward partial recovery following the initial sharp reduction of
the amplitude of WI of the VsEP recorded immediately after the cessation of
the noise exposure (Figure 2). In
nonfenestrated Sabra rats exposed to 113-dB SPL broadband noise for 2.5 minutes,
a VsEP amplitude reduction was also seen (10%-25%), but it was of short duration;
recovery was apparent within 5 minutes.13 In
the present experiment, it seems that the fenestration of the SCC allowed
a greater (60%) and longer lasting (at least 1 hour) VsEP amplitude reduction.
Thus, this study supports the hypothesis that the vestibular end organs become
more sensitive to sound stimuli (Tullio phenomenon1)
in the presence of a fenestrated SCC, which has been reported in other studies.14-15 The clinical findings in the patients
with dehiscence over the superior semicircular canal9
also demonstrate sensitivity to sound and pressure stimuli: loud sounds in
most and changes in middle ear pressure in about half induced vertigo or oscillopsia.
The symptoms resolved or improved following surgical procedures to correct
the dehiscence in 5 of the 17 patients.9 These
clinical and surgical findings provide additional support for the suggestion
that fenestration or dehiscence of a SCC allows sound and pressure stimuli
to reach and affect the vestibular end organs. In fact, Ribaric et al21-22 have taken clinical advantage of
this by fenestrating the SCC in patients with profound hearing loss and normal
vestibular function, hoping that such a procedure would enable the patients
to make use of the vestibular end organs to perceive sound stimuli. Following
fenestration, the patients reported improved hearing to bone-conducted, not
air-conducted, stimuli.
In conclusion, fenestration of the SCC makes the vestibular end organs
more sensitive to acoustic stimulation, presumably by shifting additional
acoustic energy from the cochlea to the vestibule. This finding may have clinical
significance.
AUTHOR INFORMATION
Accepted for publication October 2, 2001.
Corresponding author: Haim Sohmer, PhD, Department of Physiology,
Hebrew University-Hadassah Medical School, PO Box 12272, Jerusalem, Israel
(e-mail: sohmer{at}md2.huji.ac.il).
From the Departments of Otolaryngology–Head & Neck Surgery
(Drs Biron and Sichel) and Physiology (Drs Freeman and Sohmer), Hebrew University–Hadassah
Medical Center, Jerusalem, Israel.
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